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• W3183286935 abstract "Certain genetic variants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) are of substantial concern because they may be more transmissible or detrimentally alter the pandemic course and disease features in individual patients. SARS-CoV-2 genome sequences from 12,476 patients in the Houston Methodist health care system diagnosed from January 1 through May 31, 2021 are reported here. Prevalence of the B.1.1.7 (Alpha) variant increased rapidly and caused 63% to 90% of new cases in the latter half of May. Eleven B.1.1.7 genomes had an E484K replacement in spike protein, a change also identified in other SARS-CoV-2 lineages. Compared with non–B.1.1.7-infected patients, individuals with B.1.1.7 had a significantly lower cycle threshold (a proxy for higher virus load) and significantly higher hospitalization rate. Other variants [eg, B.1.429 and B.1.427 (Epsilon), P.1 (Gamma), P.2 (Zeta), and R.1] also increased rapidly, although the magnitude was less than that in B.1.1.7. Twenty-two patients infected with B.1.617.1 (Kappa) or B.1.617.2 (Delta) variants had a high rate of hospitalization. Breakthrough cases (n = 207) in fully vaccinated patients were caused by a heterogeneous array of virus genotypes, including many not currently designated variants of interest or concern. In the aggregate, this study delineates the trajectory of SARS-CoV-2 variants circulating in a major metropolitan area, documents B.1.1.7 as the major cause of new cases in Houston, TX, and heralds the arrival of B.1.617 variants in the metroplex. Certain genetic variants of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) are of substantial concern because they may be more transmissible or detrimentally alter the pandemic course and disease features in individual patients. SARS-CoV-2 genome sequences from 12,476 patients in the Houston Methodist health care system diagnosed from January 1 through May 31, 2021 are reported here. Prevalence of the B.1.1.7 (Alpha) variant increased rapidly and caused 63% to 90% of new cases in the latter half of May. Eleven B.1.1.7 genomes had an E484K replacement in spike protein, a change also identified in other SARS-CoV-2 lineages. Compared with non–B.1.1.7-infected patients, individuals with B.1.1.7 had a significantly lower cycle threshold (a proxy for higher virus load) and significantly higher hospitalization rate. Other variants [eg, B.1.429 and B.1.427 (Epsilon), P.1 (Gamma), P.2 (Zeta), and R.1] also increased rapidly, although the magnitude was less than that in B.1.1.7. Twenty-two patients infected with B.1.617.1 (Kappa) or B.1.617.2 (Delta) variants had a high rate of hospitalization. Breakthrough cases (n = 207) in fully vaccinated patients were caused by a heterogeneous array of virus genotypes, including many not currently designated variants of interest or concern. In the aggregate, this study delineates the trajectory of SARS-CoV-2 variants circulating in a major metropolitan area, documents B.1.1.7 as the major cause of new cases in Houston, TX, and heralds the arrival of B.1.617 variants in the metroplex. The global pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that began in early 2020 has been challenging for every academic health center and health system, hospital, and public health system in the United States and countries worldwide.1Huang C. Wang Y. Li X. Ren L. Zhao J. Hu Y. Zhang L. Fan G. Xu J. Gu X. Cheng Z. Yu T. Xia J. Wei Y. Wu W. Xie X. Yin W. Li H. Liu M. Xiao Y. Gao H. Guo L. Xie J. Wang G. Jiang R. Gao Z. Jin Q. Wang J. Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China.Lancet. 2020; 395: 497-506Abstract Full Text Full Text PDF PubMed Scopus (30327) Google Scholar, 2Zhu N. Zhang D. Wang W. Li X. Yang B. Song J. Zhao X. Huang B. Shi W. Lu R. Niu P. Zhan F. Ma X. Wang D. Xu W. Wu G. Gao G.F. Tan W. China Novel Coronavirus I. Research T. A novel coronavirus from patients with pneumonia in China, 2019.N Engl J Med. 2020; 382: 727-733Crossref PubMed Scopus (17095) Google Scholar, 3Chan J.F. Yuan S. Kok K.H. To K.K. Chu H. Yang J. Xing F. Liu J. Yip C.C. Poon R.W. Tsoi H.W. Lo S.K. Chan K.H. Poon V.K. Chan W.M. Ip J.D. Cai J.P. Cheng V.C. Chen H. Hui C.K. Yuen K.Y. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster.Lancet. 2020; 395: 514-523Abstract Full Text Full Text PDF PubMed Scopus (5853) Google Scholar, 4Wu F. Zhao S. Yu B. Chen Y.M. Wang W. Song Z.G. Hu Y. Tao Z.W. Tian J.H. 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Country-level factors associated with the early spread of COVID-19 cases at 5, 10 and 15 days since the onset.Glob Public Health. 2020; 15: 1589-1602Crossref PubMed Scopus (23) Google Scholar The pandemic has also provided unprecedented opportunities for basic and translational research in all biomedical fields. Molecular population genomics of SARS-CoV-2 were systematically analyzed in the ethnically and socioeconomically diverse metropolitan Houston, TX, area (population 7 million) since the first coronavirus disease 2019 (COVID-19) cases were reported in early March 2020.8Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.R. Shukla M. Nguyen M. Ojeda Saavedra M. Cantu C.C. Yerramilli P. Pruitt L. Subedi S. Hendrickson H. Eskandari G. Kumaraswami M. McLellan J.S. Musser J.M. Molecular architecture of early dissemination and evolution of the SARS-CoV-2 virus in metropolitan Houston, Texas.bioRxiv. 2020; 11 (e02707-20)Google Scholar, 9Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.J. Shukla M. Nguyen M. Saavedra M.O. Yerramilli P. Pruitt L. Subedi S. Kuo H.C. Hendrickson H. Eskandari G. Nguyen H.A.T. Long J.H. Kumaraswami M. Goike J. Boutz D. Gollihar J. McLellan J.S. Chou C.W. Javanmardi K. Finkelstein I.J. Musser J.M. Molecular architecture of early dissemination and massive second wave of the SARS-CoV-2 virus in a major metropolitan area.MBio. 2020; 11: e02707-e02720Crossref PubMed Scopus (69) Google Scholar, 10Long S.W. Olsen R.J. Christensen P.A. Subedi S. Olson R. Davis J.J. Saavedra M.O. Yerramilli P. Pruitt L. Reppond K. Shyer M.N. Cambric J. Finkelstein I.J. Gollihar J. Musser J.M. Sequence analysis of 20,453 severe acute respiratory syndrome coronavirus 2 genomes from the Houston metropolitan area identifies the emergence and widespread distribution of multiple isolates of all major variants of concern.Am J Pathol. 2021; 191: 983-992Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 11Musser J.M. Olsen R.J. Christensen P.A. Long S.W. Subedi S. Davis J.J. Gollihar J. Rapid, widespread, and preferential increase of SARS-CoV-2 B.1.1.7 variant in Houston, TX, revealed by 8,857 genome sequences.medRxiv. 2021; ([Preprint] doi:10.1101/2021.03.16.21253753)Google Scholar These studies are facilitated by a central molecular diagnostic laboratory that comprehensively identifies and retains all COVID-19 diagnostic specimens from our large health care system, which includes eight hospitals, emergency care clinics, and outpatient centers distributed throughout the metropolitan region. In addition, the longstanding interest in pathogen genomics and sequencing infrastructure was leveraged to investigate the spread of SARS-CoV-2 in metropolitan Houston.8Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.R. Shukla M. Nguyen M. Ojeda Saavedra M. Cantu C.C. Yerramilli P. Pruitt L. Subedi S. Hendrickson H. Eskandari G. Kumaraswami M. McLellan J.S. Musser J.M. Molecular architecture of early dissemination and evolution of the SARS-CoV-2 virus in metropolitan Houston, Texas.bioRxiv. 2020; 11 (e02707-20)Google Scholar, 9Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.J. Shukla M. Nguyen M. Saavedra M.O. Yerramilli P. Pruitt L. Subedi S. Kuo H.C. Hendrickson H. Eskandari G. Nguyen H.A.T. Long J.H. Kumaraswami M. Goike J. Boutz D. Gollihar J. McLellan J.S. Chou C.W. Javanmardi K. Finkelstein I.J. Musser J.M. Molecular architecture of early dissemination and massive second wave of the SARS-CoV-2 virus in a major metropolitan area.MBio. 2020; 11: e02707-e02720Crossref PubMed Scopus (69) Google Scholar, 10Long S.W. Olsen R.J. Christensen P.A. Subedi S. Olson R. Davis J.J. Saavedra M.O. Yerramilli P. Pruitt L. Reppond K. Shyer M.N. Cambric J. Finkelstein I.J. Gollihar J. Musser J.M. Sequence analysis of 20,453 severe acute respiratory syndrome coronavirus 2 genomes from the Houston metropolitan area identifies the emergence and widespread distribution of multiple isolates of all major variants of concern.Am J Pathol. 2021; 191: 983-992Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 11Musser J.M. Olsen R.J. Christensen P.A. Long S.W. Subedi S. Davis J.J. Gollihar J. Rapid, widespread, and preferential increase of SARS-CoV-2 B.1.1.7 variant in Houston, TX, revealed by 8,857 genome sequences.medRxiv. 2021; ([Preprint] doi:10.1101/2021.03.16.21253753)Google Scholar, 12Long S.W. Olsen R.J. Eagar T.N. Beres S.B. Zhao P. Davis J.J. Brettin T. Xia F. Musser J.M. Population genomic analysis of 1,777 extended-spectrum beta-lactamase-producing Klebsiella pneumoniae isolates, Houston, Texas: unexpected abundance of clonal group 307.MBio. 2017; 8: e00489-17Crossref PubMed Scopus (76) Google Scholar, 13Long S.W. Beres S.B. Olsen R.J. Musser J.M. 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Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3,615 genome sequences.Proc Natl Acad Sci U S A. 2014; 111: E1768-E1776Crossref PubMed Scopus (191) Google Scholar, 16Kachroo P. Eraso J.M. Beres S.B. Olsen R.J. Zhu L. Nasser W. Bernard P.E. Cantu C.C. Saavedra M.O. Arredondo M.J. Strope B. Do H. Kumaraswami M. Vuopio J. Grondahl-Yli-Hannuksela K. Kristinsson K.G. Gottfredsson M. Pesonen M. Pensar J. Davenport E.R. Clark A.G. Corander J. Caugant D.A. Gaini S. Magnussen M.D. Kubiak S.L. Nguyen H.A.T. Long S.W. Porter A.R. DeLeo F.R. Musser J.M. Integrated analysis of population genomics, transcriptomics and virulence provides novel insights into Streptococcus pyogenes pathogenesis.Nat Genet. 2019; 51: 548-559Crossref PubMed Scopus (43) Google Scholar SARS-CoV-2 viruses causing infections in the earliest phase of the pandemic affecting Houston had substantial genomic diversity and are progeny of strains derived from several continents, including Europe and Asia.8Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.R. Shukla M. Nguyen M. Ojeda Saavedra M. Cantu C.C. Yerramilli P. Pruitt L. Subedi S. Hendrickson H. Eskandari G. Kumaraswami M. McLellan J.S. Musser J.M. Molecular architecture of early dissemination and evolution of the SARS-CoV-2 virus in metropolitan Houston, Texas.bioRxiv. 2020; 11 (e02707-20)Google Scholar,9Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.J. Shukla M. Nguyen M. Saavedra M.O. Yerramilli P. Pruitt L. Subedi S. Kuo H.C. Hendrickson H. Eskandari G. Nguyen H.A.T. Long J.H. Kumaraswami M. Goike J. Boutz D. Gollihar J. McLellan J.S. Chou C.W. Javanmardi K. Finkelstein I.J. Musser J.M. Molecular architecture of early dissemination and massive second wave of the SARS-CoV-2 virus in a major metropolitan area.MBio. 2020; 11: e02707-e02720Crossref PubMed Scopus (69) Google Scholar These findings indicated that SARS-CoV-2 was introduced into our region many times independently by individuals who had traveled from different parts of the country and the world. Subsequently, sequence analysis of 5085 genomes causing the first disease wave and massive second disease wave in Houston showed that all strains in the second wave had a D614G amino acid replacement in the spike protein.9Long S.W. Olsen R.J. Christensen P.A. Bernard D.W. Davis J.J. Shukla M. Nguyen M. Saavedra M.O. Yerramilli P. Pruitt L. Subedi S. Kuo H.C. Hendrickson H. Eskandari G. Nguyen H.A.T. Long J.H. Kumaraswami M. Goike J. Boutz D. Gollihar J. McLellan J.S. Chou C.W. Javanmardi K. Finkelstein I.J. Musser J.M. Molecular architecture of early dissemination and massive second wave of the SARS-CoV-2 virus in a major metropolitan area.MBio. 2020; 11: e02707-e02720Crossref PubMed Scopus (69) Google Scholar The D614G polymorphism increases human transmission and infectivity in vitro and in vivo in animal infection models.17Korber B. Fischer W.M. Gnanakaran S. Yoon H. Theiler J. Abfalterer W. Hengartner N. Giorgi E.E. Bhattacharya T. Foley B. Hastie K.M. Parker M.D. Partridge D.G. Evans C.M. Freeman T.M. de Silva T.I. Sheffield C.-G.G. McDanal C. Perez L.G. Tang H. Moon-Walker A. Whelan S.P. LaBranche C.C. Saphire E.O. Montefiori D.C. Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 virus.Cell. 2020; 182: 812-827.e19Abstract Full Text Full Text PDF PubMed Scopus (2459) Google Scholar, 18Plante J.A. Liu Y. Liu J. Xia H. Johnson B.A. Lokugamage K.G. Zhang X. Muruato A.E. Zou J. Fontes-Garfias C.R. Mirchandani D. Scharton D. Bilello J.P. 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One of the key goals since the start of the pandemic has been to sequence all positive SARS-CoV-2 specimens from patients in our hospital system and rapidly identify mutations that may be associated with detrimental patient outcome, including therapeutic or vaccine failure. Similarly, with the recognition of an increasing number of SARS-CoV-2 variants of interest (VOIs) and variants of concern (VOCs) by public health agencies, such as the US CDC, World Health Organization, and Public Health England (https://www.cdc.gov/coronavirus/2019-ncov/cases-updates/variant-surveillance/variant-info.html, last accessed June 8, 2021; and https://www.gov.uk/government/collections/new-sars-cov-2-variant, last accessed June 8, 2021), there is now substantial domestic and international need to identify these virus genotypes rapidly and understand their velocity and patterns of dissemination. In particular, VOC B.1.1.7 (also termed Alpha), first identified in the United Kingdom, is of special interest because it has the ability to transmit effectively, it can spread through populations rapidly, and has been reported to have a significantly higher mortality rate than non-B.1.1.7 infections (Virological, https://virological.org/t/preliminary-genomic-characterisation- of-an-emergent-sars-cov-2-lineage-in-the-uk-defined-by-a-novel-set-of-spike-mutations/563, last accessed June 8, 2021; Public Health England, https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/947048/technical_briefing_voc_sh_njl2_sh2.pdf, last accessed June 8, 2021; New and Emerging Respiratory Virus Threats Advisory Group, https://app.box.com/s/3lkcbxepqixkg4mv640dpvvg978ixjtf/file/756963730457, last accessed June 8, 2021; Centre for Mathematical Modelling of Infectious Diseases, https://cmmid.github.io/topics/covid19/uk-novel-variant.html, last accessed June 8, 2021; and https://virological.org/t/lineage-specific-growth-of-sars-cov-2-b-1-1-7-during-the-english-national-lockdown/575, last accessed June 8, 2021).23Grubaugh N.D. 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Effect of natural mutations of SARS-CoV-2 on spike structure, conformation and antigenicity.Science. 2021; 373: eabi6226Crossref PubMed Scopus (182) Google Scholar Recently, two additional VOIs, B.1.427 and B.1.429 (Epsilon), were recognized by the CDC in part because of their rapid transmission in many California communities41Zhang W. Davis B.D. Chen S.S. Sincuir Martinez J.M. Plummer J.T. Vail E. Emergence of a novel SARS-CoV-2 variant in southern California.JAMA. 2021; 325: 1324-1326Crossref PubMed Scopus (207) Google Scholar (Outbreak.info, https://outbreak.info/situation-reports?pango=b.1.427, last accessed June 8, 2021; and https://outbreak.info/situation-reports?pango=b.1.4279, last accessed June 8, 2021). Based on sequencing 20,453 SARS-CoV-2 genomes causing COVID-19 disease in Houston, all named VOIs and VOCs are circulating in the metropolitan region, making it the first community to document their presence.10Long S.W. Olsen R.J. Christensen P.A. Subedi S. Olson R. Davis J.J. Saavedra M.O. Yerramilli P. Pruitt L. Reppond K. Shyer M.N. Cambric J. Finkelstein I.J. Gollihar J. Musser J.M. Sequence analysis of 20,453 severe acute respiratory syndrome coronavirus 2 genomes from the Houston metropolitan area identifies the emergence and widespread distribution of multiple isolates of all major variants of concern.Am J Pathol. 2021; 191: 983-992Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar A follow-up study reported rapid increase of VOC UK B.1.1.7 in Houston11Musser J.M. Olsen R.J. Christensen P.A. Long S.W. Subedi S. Davis J.J. Gollihar J. Rapid, widespread, and preferential increase of SARS-CoV-2 B.1.1.7 variant in Houston, TX, revealed by 8,857 genome sequences.medRxiv. 2021; ([Preprint] doi:10.1101/2021.03.16.21253753)Google Scholar; cases infected with the variant were estimated to have a doubling time of approximately 7 days. This rapid B.1.1.7 growth trajectory raised the possibility that this variant would cause nearly all new COVID-19 cases in metropolitan Houston by the end of March or early April 2021, a time frame similar to an estimate made in late January by the CDC.33Galloway S.E. Paul P. MacCannell D.R. Johansson M.A. Brooks J.T. MacNeil A. Slayton R.B. Tong S. Silk B.J. Armstrong G.L. Biggerstaff M. Dugan V.G. Emergence of SARS-CoV-2 B.1.1.7 lineage - United States, December 29, 2020-January 12, 2021.MMWR Morb Mortal Wkly Rep. 2021; 70: 95-99Crossref PubMed Google Scholar This study reports integrated virus genome and patient data for 12,476 unique COVID-19 cases identified between January 1, 2021, and May 31, 2021, including 3276 patients with the B.1.1.7 VOC. In the latter half of May, depending on the day, 63% to 90% of all new COVID-19 cases in metropolitan Houston were caused by B.1.1.7. Linked medical record information, available for virtually all sequenced genomes, was used to study the relationship between virus genotypes and patient phenotypes. Patients infected with B.1.1.7 had significantly lower cycle threshold (CT) values in nasopharyngeal specimens (considered to be a proxy for higher virus load) and a significantly higher hospitalization rate compared with non-B.1.1.7 patients. There was no difference between these two groups in hospital length of stay or mortality. Of the 3276 B.1.1.7 genomes, 11 (0.3%) had an E484K change in spike protein that reduces binding by some neutralizing antibodies. Unexpectedly, five cases of B.1.1.7 were detected from samples collected in early December, resulting in a revised time frame for the introduction of this variant to Houston. Twenty-two patients were identified with COVID-19 caused by B.1.617.1 (Kappa) or B.1.617.2 (Delta) variants reported to be causing widespread disease and extensive public health problems in India, other Southeast Asian countries, and many regions of the United Kingdom (World Health Organization, https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid-19---8-june-2021, last accessed June 9, 2021).42Cherian S. Potdar V. Jadhav S. Yadav P. Gupta N. Das M. Rakshit P. Singh S. Abraham P. Panda S. Convergent evolution of SARS-CoV-2 spike mutations, L452R, E484Q and P681R, in the second wave of COVID-19 in Maharashtra, India.bioRxiv. 2021; ([Preprint] doi:10.1101/2021.04.22.440932)Google Scholar, 43Yadav P.D. Sapkal G.N. Abraham P. Ella R. Deshpande G. Patil D.Y. Nyayanit D.A. Gupta N. Sahay R.R. Shete A.M. Panda S. Bhargava B. Mohan V.K. Neutralization of variant under investigation B.1.617 with sera of BBV152 vaccinees.Clin Infect Dis. 2021; : ciab411Crossref PubMed Scopus (101) Google Scholar, 44Yadav P.D. Mohandas S. Shete A.M. Nyayanit D.A. Gupta N. Patil D.Y. Sapkal G.N. Potdar V. Kadam M. Kumar A. Kumar S. Suryavanshi D. Mote C.S. Abraham P. Panda S. Bhargava B. SARS CoV-2 variant B.1.617.1 is highly pathogenic in hamsters than B.1 variant.bioRxiv. 2021; ([Preprint] doi:10.1101/2021.05.05.442760)PubMed Google Scholar, 45Hoffmann M. Hofmann-Winkler H. Krüger N. Kempf A. Nehlmeier I. Graichen L. Sidarovich A. Moldenhauer A.-S. Winkler M.S. Schulz S. Jäck H.-M. Stankov M.V. Behrens G.M.N. Pöhlmann S. SARS-CoV-2 variant B.1.617 is resistant to bamlanivimab and evades antibodies induced by infection and vaccination.Cell Rep. 2021; 36: 109415Abstract Full Text Full Text PDF PubMed Scopus (138) Google Scholar, 46Ferreira I. Datir R. Kemp S. Papa G. Rakshit P. Singh S. et al.The Indian SARS-CoV-2 Genomics Consortium (INSACOG); The CITIID-NIHR BioResource COVID-19 Collaboration; The Genotype to Phenotyp" @default.
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